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Characteristics of a Copper-cadmium Tolerant Strain Screened from Tailings and Its Potential in Remediation of Heavy Metal Contaminated Soil

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Abstract

In this study, we have screened out a copper-cadmium tolerant strain K1 from the farmland soil of Laoyaling tailings in Tongling City, Anhui Province, China. The strain was identified as Pseudomonas aeruginosa by 16S rDNA sequencing. To reveal its influence on pollution remediation, the growth characteristics of strain K1 and its effects on soil properties were analyzed. The minimum inhibitory concentration (MIC) of strain K1 toward copper and cadmium was 996.70 mg·L−1 and 313.81 mg·L−1, respectively. The optimal growth pH of K1 strain was 7.0 and the optimal temperature was 30℃. Interestingly, we found that the growth of strain K1 increased the environmental pH. The removal rates of copper and cadmium in solution by the stain were 32.44% and 34.05%, respectively. By application of strain K1, the soil electrical conductivity (EC) reduced from 0.46 ms·cm−1 to 0.40 ms·cm−1; the contents of available copper and cadmium in the soil decreased by 34.89% and 17.88%; the activities of soil catalase and invertase were also significantly improved. In conclusion, the indigenous strain K1 showed significant resistance to heavy metals and could be expected to be used as a potential remediation agent or phytoremediation enhancer toward the heavy metal contaminated soil in tailings.

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References

  • Agnello, A. C., Bagard, M., Van Hullebusch, E. D., Esposito, G., & Huguenot, D. (2016). Comparative bioremediation of heavy metals and petroleum hydrocarbons co-contaminated soil by natural attenuation, phytoremediation, bioaugmentation and bioaugmentation-assisted phytoremediation. Science of the Total Environment, 563, 693–703.

    Article  Google Scholar 

  • Andrews, J. M. (2001). Determination of minimum inhibitory concentrations. Journal of Antimicrobial Chemotherapy, 48, 5–16.

    Article  CAS  Google Scholar 

  • Arif, M. S., Riaz, M., Shahzad, S. M., Yasmeen, T., Akhtar, M. J., Riaz, M. A., Jassey, V. E. J., Bragazza, L., & Buttler, A. (2016). Associative interplay of plant growth promoting rhizobacteria (Pseudomonas aeruginosa QS40) with nitrogen fertilizers improves sunflower (Helianthus annuus L.) productivity and fertility of aridisol. Applied Soil Ecology, 108, 238–247.

    Article  Google Scholar 

  • Bensidhoum, L., Nabti, E., Tabli, N., Kupferschmied, P., Weiss, A., Rothballer, M., Schmid, M., Keel, C., & Hartmann, A. (2016). Heavy metal tolerant Pseudomonas protegens isolates from agricultural well water in northeastern Algeria with plant growth promoting, insecticidal and antifungal activities. European Journal of Soil Biology, 75, 38–46.

    Article  CAS  Google Scholar 

  • Chellaiah, E. R. (2018). Cadmium (heavy metals) bioremediation by Pseudomonas aeruginosa: A minireview. Applied Water Science, 8(6), 254.

    Article  Google Scholar 

  • Chibuike, G. U., & Obiora, S. C. (2014). Heavy metal polluted soils: Effect on plants and bioremediation methods. Applied and Environmental Soil Science, 2014, 752708.

    Article  Google Scholar 

  • Das, S., Dash, H. R., & Chakraborty, J. (2016). Genetic basis and importance of metal resistant genes in bacteria for bioremediation of contaminated environments with toxic metal pollutants. Applied Microbiology and Biotechnology, 100, 2967–2984.

    Article  CAS  Google Scholar 

  • Dong, X.J., & Chen, W.H. (2002). Screening of bacteria of Cu2+-tolerant strain and its optimized adsorption conditions. Environmental Scicence & Technology, 25(5): 6–7, 19.

  • Dresler, S., Hawrylak-Nowak, B., Kováčik, J., Pochwatka, M., Hanaka, A., Strzemski, M., Sowa, I., & Wójciak-Kosior, M. (2019). Allantoin attenuates cadmium-induced toxicity in cucumber plants. Ecotoxicological and Environmental Safety, 170, 120–126.

    Article  CAS  Google Scholar 

  • Fashola, M. O., Ngole-Jeme, V. M., & Babalola, O. O. (2016). Heavy metal pollution from gold mines: Environmental effects and bacterial strategies for resistance. International Journal of Environmental Research and Public Health, 13, 1047.

    Article  Google Scholar 

  • Ferris, F. G., Schultze, S., Witten, T. C., Fyfe, W. S., & Beveridge, T. J. (1989). Metal interactions with microbial biofilms in acidic and neutral pH environments. Applied and Environmental Microbiology, 55(5), 1249–1257.

    Article  CAS  Google Scholar 

  • Fu, D. H., Xue, Z. H., Yao, Y. L., Zeng, T. Y., & Lu, X. Y. (2012). Screen and identification of high copper-resisting fungi and its application in absorbing copper from tea garden soil. Chinese Agricultural Science Bulletin, 28(34), 268–273.

    Google Scholar 

  • Geng, Y. Y., Wang, X. M., Wang, H. Q., & Tong, X. M. (2010). Screening and identification of cadmium -tolerant bacteria in polluted soil and characteristics. Journal of Northeast Agricultural University (english Edition), 41(11), 59–65.

    CAS  Google Scholar 

  • Guan, S.Y. (Eds.). (1986). Soil enzymes and their research methods. China Agricultural Press, Beijing

  • Gupta, V., Kumar, G. N., & Buch, A. (2020). Colonization by multi-potential Pseudomonas aeruginosa P4 stimulates peanut (Arachis hypogaea L.) growth, defence physiology and root system functioning to benefit the root-rhizobacterial interface. Journal of Plant Physiology, 248, 153144.

    Article  CAS  Google Scholar 

  • He, D., Cui, J., Gao, M., Wang, W., Zhou, J., Yang, J., Wang, J., Li, Y., Jiang, C., & Peng, Y. (2019). Effects of soil amendments applied on cadmium availability, soil enzyme activity, and plant uptake in contaminated purple soil. Science of the Total Environment, 654, 1364–1371.

    Article  CAS  Google Scholar 

  • Herath, I., Zhao, F. J., Bundschuh, J., Wang, P., Wang, J., Ok, Y. S., Palansooriya, K. N., & Vithanage, M. (2020). Microbe mediated immobilization of arsenic in the rice rhizosphere after incorporation of silica impregnated biochar composites. Journal of Hazardous Materials, 398, 123096.

    Article  CAS  Google Scholar 

  • Hu, J.X. (2020). Study on induced mineralization and adsorption of Cd2+ by a Cd tolerant bacteria. ShenYang University of Chemical and Technology.

  • Igiri, B. E., Okoduwa, S. I. R., Idoko, G. O., Akabuogu, E. P., Adeyi, A. O., & Ejiogu, I. K. (2018). Toxicity and bioremediation of heavy metals contaminated ecosystem from Tannery wastewater: A review. Journal of Toxicology, 2018, 2568038.

    Article  Google Scholar 

  • Kang, S. M., Asaf, S., Khan, A. L., Lubna., Khan. A., Mun, B. G., Khan, M. A., Gul, H., & Lee, I. J. (2020). Complete genome sequence of Pseudomonas psychrotolerans CS51, a plant growth-promoting bacterium, under heavy metal stress conditions. Microorgamisms, 8(3), 382.

  • Kang, W. (2014) Mechanism and application of microorganism coupled with casto for remediating copper-contaminated soil. China University of Geosciences.

  • Lin, X. Y., Mou, R. X., Cao, Z. Y., Zhu, Z. W., & Chen, M. X. (2015). Isolation and cadmium adsorption mechanisms of cadmium-resistant bacteria strains. Journal of Agro-Environment Science, 34(9), 1700–1706.

    CAS  Google Scholar 

  • Lister, P. D., Wolter, D. J., & Hanson, N. D. (2009). Antibacterial-resistant Pseudomonas aeruginosa: Clinical impact and complex regulation of chromosomally encoded resistance mechanisms. Clinical Microbiology Reviews, 22(4), 582–610.

    Article  CAS  Google Scholar 

  • Liu, T.T., & Teng, J.T. (2019). Screening and separation of copper resistant microorganisms in copper contaminated soil. Journal of Anhui Agricultural Science, 47(2): 60–63, 102.

  • Liu, Y.L. (2018). Isolation of a Cd-resistant bacterium and its effect on cadmium accumulation in rice (Oryza sativa L.). Hunan Agricultural University.

  • Luo, Z. H., Tian, F., & Wei, Y. T. (2020). Study on screening and adsorption characteristics of copper ion resistance bacteria. Guangxi Sciences, 27(1), 57–64.

    Google Scholar 

  • Ma, H., Wei, M., Wang, Z., Hou, S., Li, X., & Xu, H. (2020a). Bioremediation of cadmium polluted soil using a novel cadmium immobilizing plant growth promotion strain Bacillus sp. TZ5 loaded on biochar. Journal of Hazardous Materials, 388, 122065.

    Article  CAS  Google Scholar 

  • Ma, Y., Wang, Y., Chen, Q., Li, Y., Guo, D., Nie, X., & Peng, X. (2020b). Assessment of heavy metal pollution and the effect on bacterial community in acidic and neutral soils. Ecological Indicators, 117, 106626.

    Article  CAS  Google Scholar 

  • Mekwichai, P., Tongcumpou, C., Kittipongvises, S., & Tuntiwiwattanapun, N. (2020). Simultaneous biosurfactant-assisted remediation and corn cultivation on cadmium-contaminated soil. Ecotoxicological and Environmental Safety, 192.

  • Mesa-Marín, J., Pérez-Romero, J. A., Redondo-Gómez, S., Pajuelo, E., Rodríguez-Llorente, I. D., & Mateos-Naranjo, E. (2020). Impact of plant growth promoting bacteria on Salicornia ramosissima ecophysiology and heavy metal phytoremediation capacity in estuarine soils. Frontiers in Microbiology, 11, 553018.

    Article  Google Scholar 

  • Mima, T., Kohira, N., Li, Y., Sekiya, H., Ogawa, W., Kuroda, T., & Tsuchiya, T. (2009). Gene cloning and characteristics of the RND-type multidrug efflux pump MuxABC-OpmB possessing two RND components in Pseudomonas aeruginosa. Microbiology, 155(Pt11), 3509–3517.

    Article  CAS  Google Scholar 

  • Minaxi, & Saxena, J. (2010). Characterization of Pseudomonas aeruginosa RM-3 as a potential biocontrol agent. Mycopathologia, 170(3), 181–193.

    Article  CAS  Google Scholar 

  • Naik, M. M., & Dubey, S. K. (2011). Lead-enhanced siderophore production and alteration in cell morphology in a Pb-resistant Pseudomonas aeruginosa strain 4EA. Current Microbiology, 62, 409–414.

    Article  CAS  Google Scholar 

  • Naranjargal, S., Chen, G. Q., Chen, Z. Y., Li, S. S., Narantuya, D., Battsetseg, C., & Zhong, W. H. (2019). Screening, identification, and performance of heavy metal resistant bacteria from gold mine soil. Chemistry & Bioengineering, 36(8), 31–36.

    Google Scholar 

  • Oves, M., Khan, M. S., & Zaidi, A. (2013). Chromium reducing and plant growth promoting novel strain Pseudomonas aeruginosa OSG41 enhance chickpea growth in chromium amended soils. European Journal of Soil Biology, 56, 72–83.

    Article  CAS  Google Scholar 

  • Peng, W., Li, X., Song, J., Jiang, W., Liu, Y., & Fan, W. (2018). Bioremediation of cadmium and zinc-contaminated soil using Rhodobacter sphaeroides. Chemosphere, 197, 33–41.

    Article  CAS  Google Scholar 

  • Rahman, M. F., Ghosal, A., Alam, M. F., & Kabir, A. H. (2017). Remediation of cadmium toxicity in field peas (Pisum sativum L.) through exogenous silicon. Ecotoxicological and Environmental Safety, 135, 165–172.

    Article  CAS  Google Scholar 

  • Remacle, J., Muguruza, I., & Fransolet, M. (1992). Cadmium removal by a strain of Alcaligenes denitrificans isolated from a metal-polluted pond. Water Research, 26(7), 923–926.

    Article  CAS  Google Scholar 

  • Ren, X. M., Guo, S. J., Tian, W., Chen, Y., Han, H., Chen, E., Li, B. L., Li, Y. Y., & Chen, Z. J. (2019). Effects of plant growth-promoting bacteria (PGPB) inoculation on the growth, antioxidant activity, Cu uptake, and bacterial community structure of Rape (Brassicanapus L.) grown in Cu-contaminated agricultural soil. Front Microbiol, 10, 1455.

    Article  Google Scholar 

  • Saha, J., Sarkar, M., Mandal, P., & Pal, A. (2022). Comparative study of heavy metal uptake and analysis of plant growth promotion potential of multiple heavy metal-resistant bacteria isolated from arable land. Current Microbiology, 79, 7.

    Article  CAS  Google Scholar 

  • Schalk, I. J., Hannauer, M., & Braud, A. (2011). New roles for bacterial siderophores in metal transport and tolerance. Environmental Microbiology, 13(11), 2844–2854.

    Article  CAS  Google Scholar 

  • Shen, Q. Y., Cao, Z. Q., Zhu, Y. F., & Shi, W. L. (2016). Isolation of a Cd-resistant bacterium and optimization of its bio-accumulation condition. Soils, 48(03), 615–620.

    Google Scholar 

  • Shi, G. Y., Cheng, Y. Y., Shi, Q., & Shi, W. L. (2017). Study of the biosorption of copper and lead by Pseudomonas aeruginosa. Acta Scientiae Circumstantiae, 37(6), 2107–2113.

    CAS  Google Scholar 

  • Shi, G. Y., Hu, J. Y., Ding, F. Q., Li, S. Q., Shi, W. L., & Chen, Y. (2022). Exogenous Pseudomonas aeruginosa application improved the phytoremediation efficiency of Lolium multiflorum Lam on Cu–Cd co-contaminated soil. Environmental Technology & Innovation, 27, 102489.

    Article  CAS  Google Scholar 

  • Sinha, S., & Mukherjee, S. K. (2008). Cadmium-induced siderophore production by a high Cd-resistant bacterial strain relieved Cd toxicity in plants through root colonization. Current Microbiology, 56(1), 55–60.

    Article  CAS  Google Scholar 

  • Song, J., Shen, Q., Wang, L., Qiu, G., Shi, J., Xu, J., Brookes, P. C., & Liu, X. (2018). Effects of Cd, Cu, Zn and their combined action on microbial biomass and bacterial community structure. Environmental Pollution, 243, 510–518.

    Article  CAS  Google Scholar 

  • Tu, C., Wei, J., Guan, F., Liu, Y., Sun, Y. H., & Luo, Y. M. (2020). Biochar and bacteria inoculated biochar enhanced Cd and Cu immobilization and enzymatic activity in a polluted soil. Environment International, 137, 105576.

    Article  CAS  Google Scholar 

  • Wallenstein, M.D., & Burns, R.G. (2011). Ecology of extracellular enzyme activities and organic matter degradation in soil: a complex community-driven process. John Wiley & Sons, Ltd.

  • Wang, H. O., Zhong, G. R., Wang, L. M., Ai, Y., Ren, J., & Zhi, R. (2011). Identification of a copper-resistant bacteria and its accumulation ability. Chinese Journal of Environmental Engineering, 5(10), 2380–2384.

    CAS  Google Scholar 

  • Wang, Y.B. (Eds.). (2020). Experimental technology for ecological remediation of soil pollution. Science Press, Beijing.

  • Wang, Y. B., Zhang, L. Q., & Liu, D. Y. (2004). Heavy metals accumulation in different parts of Paeonia ostii and soils at copper tailings yard. Chinese Journal of Applied Ecology, 15(12), 2351–2354.

    CAS  Google Scholar 

  • Wyszkowska, J., Borowik, A., Kucharski, M., & Kucharski, J. (2013). Effect of cadmium, copper and zinc on plants, soil microorganisms and soil enzymes. Journal of Elementology, 18, 769–796.

    Google Scholar 

  • Xia, S., Song, Z., Jeyakumar, P., Shaheen, S. M., Rinklebe, J., Ok, Y. S., Bolan, N., & Wang, H. (2019). A critical review on bioremediation technologies for Cr(VI)-contaminated soils and wastewater. Critical Reviews in Environmental Science & Technology, 49, 1027–1078.

    Article  CAS  Google Scholar 

  • Yin, H., He, B., Peng, H., Ye, J., Yang, F., & Zhang, N. (2008). Removal of Cr(VI) and Ni( II) from aqueous solution by fused yeast: Study of cations release and biosorption mechanism. Journal of Hazardous Materials, 158(2/3), 568–576.

    Article  CAS  Google Scholar 

  • Ying, J. Y., Yuan, H. L., & Li, B. Z. (2003). The cadmium resistance mechanisms of Phoma strain. China Environmental Science, 23(6), 575–578.

    CAS  Google Scholar 

  • Yu, X. M., Peng, S. M., Wang, H. T., Fu, Y., Li, J., & Zhang, S. (2019). Adsorption mechanism of Cd2+ by cadmium tolerant Bacillus. Jiangsu Agricultural Sciences, 47(20), 293–297.

    Google Scholar 

  • Zeng, W., Li, F., Wu, C., Yu, R., Wu, X., Shen, L., Liu, Y., Qiu, G., & Li, J. (2020). Role of extracellular polymeric substance (EPS) in toxicity response of soil bacteria Bacillus sp. S3 to multiple heavy metals. Bioprocess and Biosystems Engineering, 43, 153–167.

    Article  CAS  Google Scholar 

  • Zhang, X., Dou, Y., Gao, C., He, C., Gao, J., Zhao, S., & Deng, L. (2019). Removal of Cd (II) by modified maifanite coated with Mg-layered double hydroxides in constructed rapid infiltration systems. Science of the Total Environment, 685, 951–962.

    Article  CAS  Google Scholar 

  • Zhang, Y. X., Wang, J., Chai, T. Y., Zhang, Q., Liu, J. G., Li, X., Bai, Z. Q., & Su, Z. J. (2012). Mechanism of heavy-metal tolerance in Pseudomonas aeruginosa ZGKD2. Environmental Science, 33(10), 3613–3619.

    Google Scholar 

  • Zhang, Y. X., Yu, S., Wen, Z. S., Bai, L., & Li, X. (2009). Bioremediation technology for heavy-metal contaminated soil. Metal Mine, 394(4), 146–149.

    Google Scholar 

  • Zhao, Q., Zhou, L. M., Zheng, X. M., Wang, Y. J., & Lu, J. M. (2015). Study on enzymatic activities and behaviors of heavy metal in sediment-plant at muddy tidal flat in Yangtze Estuary. Environmental Earth Sciences, 73(7), 3207–3216.

    Article  CAS  Google Scholar 

  • Zhao, Y., Yao, J., Yuan, Z., Wang, T., Zhang, Y., & Wang, F. (2017). Bioremediation of Cd by strain GZ-22 isolated from mine soil based on biosorption and microbially induced carbonate precipitation. Environmental Science and Pollution Research, 24, 372–380.

    Article  CAS  Google Scholar 

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Acknowledgements

The authors thank Professor Bao Lingzhi for his language proofreading of this paper.

Funding

The work was financially supported by the National Natural Science Foundation of China (31700476), the Collaborative Innovation Project of Colleges and Universities of Anhui Province (GXXT-2020–075), and the University Natural Science Research Project of Anhui Province (KJ2021A0853).

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Nannan Wang and Youbao Wang contributed to the study conception and design. Material preparation, data collection and analysis were performed by Yufan Wang, Bingbing Li, Fei Huang, Chuanhao Sun, Xintong Li, and Ran Zhao. The first draft of the manuscript was written by Nannan Wang. Youbao Wang commented on previous versions of the manuscript. Youbao Wang and Nannan Wang obtained funding. Youbao Wang is responsible for this article. All authors read and approved the final manuscript.

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Correspondence to Youbao Wang.

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Wang, N., Wang, Y., Li, B. et al. Characteristics of a Copper-cadmium Tolerant Strain Screened from Tailings and Its Potential in Remediation of Heavy Metal Contaminated Soil. Water Air Soil Pollut 234, 277 (2023). https://doi.org/10.1007/s11270-023-06296-7

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